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Diversity and Divergence of Dinoflagellate Histone Proteins

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Diversity and Divergence of Dinoflagellate Histone Proteins G3: Genes|Genomes|Genetics Early Online, published on December 8, 2015 as doi:10.1534/g3.115.023275 Diversity and divergence of dinoflagellate histone proteins Georgi K. Marinov1 and Michael Lynch1 1Department of Biology, Indiana University, Bloomington, IN 47405, United States Abstract Histone proteins and the nucleosomal organization of chromatin are near-universal eukaroytic features, with the exception of dinoflagellates. Previous studies have suggested that histones do not play a major role in the packaging of dinoflagellate genomes, although several genomic and transcriptomic surveys have detected a full set of core histone genes. Here, transcrip- tomic and genomic sequence data from multiple dinoflagellate lineages are analyzed, and the diversity of histone proteins and their variants characterized, with particular focus on their po- tential posttranslational modifications and the conservation of the histone code. In addition, the set of putative epigenetic mark readers and writers, chromatin remodelers and histone chap- erones are examined. Dinoflagellates clearly express the most derived set of histones among all autonomous eukaryote nuclei, consistent with a combination of relaxation of sequence con- straints imposed by the histone code and the presence of numerous specialized histone vari- ants. The histone code itself appears to have diverged significantly in some of its compo- nents, yet others are conserved, implying conservation of the associated biochemical processes. Specifically, and with major implications for the function of histones in dinoflagellates, the re- sults presented here strongly suggest that transcription through nucleosomal arrays happens in dinoflagellates. Finally, the plausible roles of histones in dinoflagellate nuclei are discussed. Introduction know that dinoflagellates firmly belong to the alveolates, together with apicomplexans and ciliates, and that the loss A core feature of eukaryotic genome biology is the nucleoso- of nucleosomes is a derived feature. But the mystery of mal organization of chromatin. Nucleosomes consist of a hi- dinoflagellate chromatin remains largely unresolved. stone octamer containing two copies of each of the four core Several reports have identified histone-like proteins in histone proteins H2A, H2B, H3 and H4, wrapped around dinoflagellates (Chan et al. 2006; Chan et al. 2007; Wargo ∼147 bp of DNA (Luger et al. 1997). In addition, the and Rizzo 2000; Chudnovsky et al. 2002; Sala-Rovira et linker histone H1 binds to the nucleosome and the linker al. 1991; Wong et al. 2003; Rizzo and Burghardt 1982). DNA between individual nucleosomes. More recently, it was found that dinoflagellates express The major exception from this almost universal organi- virus-derived nucleoproteins, completely unrelated to hi- zation are dinoflagellates. Dinoflagellates exhibit numerous stones (DVNPs, or Dinoflagellate Viral NucleoProteins), highly unusual features, such as the organization of their mi- which seem to substitute for histones as far as the packaging tochondrial (Waller and Jackson 2009) and plastid (Zhang of DNA is concerned (Gornik et al. 2012). However, multi- et al. 1999; Barbrook and Howe 2000) genomes, but their ple reports have also identified histone genes and low levels nuclei are particularly striking (Rizzo 2003). Dinoflagellate of histone proteins in several species. These include stud- chromatin does not exhibit a banding pattern upon nuclease ies of transcriptomes from Lingulodinium (Roy and Morse digestion, it contains little acid-soluble protein (the ratio of 2012), Symbiodinium (Bayer et al. 2012), and Alexandrium basic proteins to DNA is ∼10% compared to the typical catenella (Zhang et al. 2014), the draft genome sequence 1:1; Rizzo and Nooden 1972; Herzog and Soyer 1981; ), and of Symbiodinium minutum (Shoguchi et al. 2013), and en- chromosomes exist in a permanently condensed liquid crys- vironmental transcriptomes (Lin et al. 2010). talline state (Rill et al. 1989). Histone proteins are not readily detected in dinoflagellates, and until quite recently These observations suggest that histones do play some they were thought to be completely absent. So unusual role in dinoflagellate biology, but its precise nature remains is dinoflagellate chromatin that at one time dinoflagellates unclear. A somewhat underappreciated fact is that the were suggested to be \mesokaryotes", i.e. intermediate be- loss of nucleosomes has far more profound consequences tween prokaryotes and eukaryotes (Dodge 1965). We now than the mere packaging of DNA, as the post-translational 1 © The Author(s) 2013. Published by the Genetics Society of America. Figure 1: Detection of histones and DVNP proteins in dinoflagellate transcriptomic and genomic as- semblies. \Total" refers to the number of unique proteins detected, while \complete" refers to the subset of full-length proteins (i.e., assembled transcripts in which both start and stop codons are present). Symbiodinium minutum and Perkin- sus marinus are colored differently as genome assemblies are available for these species, while only the transcriptomic space has been sampled for all others. The dinotoms are also highlighted separately as they contain a unreduced diatom endosymbiont, meaning that their transcriptomes contains transcripts from two different eukaryotic genomes, only one of which is a dinoflagellate. The cladogram was generated following previously published phylogenies (Orr et al. 2014). modifications (PTMs) of histone proteins and the \histone been identified, densely covering histone tails (Huang et al. code" they constitute (Jenuwein and Allis 2001) play a key 2014), which is one explanation for the extreme conserva- role in most aspects of chromatin biology. These modifica- tion of their sequence across very deeply diverging lineages tions happen primarily (but not only) in the N-terminal of eukaryotes (Waterborg 2012; Postberg et al. 2010; Feng tails of histones and serve as platforms for the recruit- and Jacobsen 2011). ment of specific PTM \reader" domain-containing proteins In the light of the deep conservation and fundamental (Kouzarides 2007). Hundreds of histone modifications have importance of the histone code, it is of significant interest 2 Figure 2: Distribution of histone protein lengths in dinoflagellates. (A) Histone H2A; (B) Histone H2B; (C) Hi- stone H3; (D) Histone H4. Values for Homo sapiens, Drosophila melanogaster, Saccharomyces cerevisiae, and Arabidopsis thaliana core histones are shown at the bottom of each panel for comparison. 3 Figure 3: Expression levels of DVNP, linker histone and histone genes in dinoflagellates in TPM (Tran- scripts Per Million). (A) Alexandrium tamarense; from left to right: SRR1296765, SRR1296766, SRR1300221, SRR1300222; (B) Amphidinium carterae; from left to right: SRR1294391, SRR1294392, SRR1294393, SRR1294394, SRR1296757, SRR1296758; (C) Azadinium spinosum; from left to right: SRR1300306, SRR1300307, SRR1300308; (D) Noctiluca scintillans: SRR1296929; (E) Amoebophrya sp.: SRR1296703. See Figures S2{S7 for data for other species. 4 to know the extent to which it is conserved in dinoflagel- suggests that histone H1 is present in all dinoflagellates, lates given that histones are present but are not the major with the failures to detect it being false negatives. constituent of chromatin in these organisms. Such insights A unique representative of the complexity of dinoflagel- can shed light on the functional roles of histone proteins late biology deserves a special mention. The largest number in dinoflagellate biology. In this study, these issues are ad- of histones were identified in Durinskia baltica and Kryp- dressed by carrying out a detailed survey of the sequence toperidinium/Glenodinium foliaceum. These species are of histone proteins, as well as the presence or absence of known as \dinotoms" (Imanian et al. 2010), as they har- chromatin mark writers, readers and erasers in available bor a tertiary diatom endosymbiont (Dodge 1971; Tomas transcriptomic and genomic data from a large number of and Cox 1973; Figueroa et al. 2009), which has not been dinoflagellate species. reduced and retains a large genome. This means that they have both a dinoflagellate nucleus and a diatom one, the lat- ter with conventional nucleosomal organization. Thus, all Results results that follow should be interpreted with this caveat in mind in the case of dinotoms. Histone proteins in dinoflagellates Another potentially confounding factor concerns the pu- rity of the samples studied, many of which were not axenic Their often very large size and existing technological lim- (Table S1). In some cases, the presence of other eukaryotes itations have so far prevented the complete sequencing of is necessary to maintain dinoflagellate cultures. For ex- dinoflagellates genomes, and little is known in detail about ample, Dinophysis contains kleptoplastids of cryptophyte their sequence and organization. Fortunately, in recent origin (Schnepf and Elbr¨achter 1988; Nagai et al. 2008), years transcriptomic data from a large number of dinoflagel- which apparently do not contain a nucleomorph (Lucas and lates has become available, in particular through the efforts Vesk 1990), and are extracted from the ciliate Myrionecta of the Marine Microbial Eukaryote Transcriptome Sequenc- rubra (=Mesodinium rubra) (Takishita et al. 2002), which ing Project (MMETSP; Keeling et al. 2014). MMETSP in turn acquires them from cryptophytes (Johnson et al. transcriptome assemblies and translations served as the 2006); Dinophysis is grown together with Myrionecta.
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